The EBAX-type Cullin-RING E3 Ligase and Hsp90 Guard the Protein Quality of the SAX-3/Robo Receptor in Developing Neurons

Neuron

Volumn 79, Issue 5, 2013, Pages 903-916

  Wang, Zhiping ^a   Hou, Yanli ^c   Guo, Xing ^b   vanderVoet, Monique ^d   Boxem, Mike ^d   Dixon, JackE ^b,c   Chisholm, AndrewD ^a   Jin, Yishi ^a,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b San Diego   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DAF 21 PROTEIN; EBAX 1 PROTEIN; EBAX TYPE CULLIN RING E3 LIGASE; HEAT SHOCK PROTEIN 90; LIGASE; REGULATOR PROTEIN; ROBO3 PROTEIN; ROUNDABOUT RECEPTOR; SAX 3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EMBRYO; ENZYME SUBSTRATE; GAZE PARALYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL DIFFERENTIATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN QUALITY CONTROL; QUALITY CONTROL; SCOLIOSIS; TEMPERATURE; VERTEBRATE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CULLIN PROTEINS; DROSOPHILA; HSP90 HEAT-SHOCK PROTEINS; MICE; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NEUROGENESIS; NEURONS; RECEPTORS, IMMUNOLOGIC; UBIQUITIN-PROTEIN LIGASES;

EID: 84884184064     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.06.035     Document Type: Article

References (50)

1. Birnby D.A., Link E.M., Vowels J.J., Tian H., Colacurcio P.L., Thomas J.H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in caenorhabditis elegans. Genetics 2000, 155:85-104.
2. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
3. Buchberger A., Bukau B., Sommer T. Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol. Cell 2010, 40:238-252.
4. Burga A., Casanueva M.O., Lehner B. Predicting mutation outcome from early stochastic variation in genetic interaction partners. Nature 2011, 480:250-253.
5. Claessen J.H., Kundrat L., Ploegh H.L. Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol. 2012, 22:22-32.
6. Deng H.X., Chen W., Hong S.T., Boycott K.M., Gorrie G.H., Siddique N., Yang Y., Fecto F., Shi Y., Zhai H., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
7. Desai C., Garriga G., McIntire S.L., Horvitz H.R. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 1988, 336:638-646.
8. Dickson B.J., Gilestro G.F. Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu. Rev. Cell Dev. Biol. 2006, 22:651-675.
9. Edwards M.J., Saunders R.D., Shiota K. Effects of heat on embryos and foetuses. Int. J. Hyperthermia 2003, 19:295-324.
10. Evgrafov O.V., Mersiyanova I., Irobi J., Van Den Bosch L., Dierick I., Leung C.L., Schagina O., Verpoorten N., Van Impe K., Fedotov V., et al. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat. Genet. 2004, 36:602-606.
11. Fleming T., Chien S.C., Vanderzalm P.J., Dell M., Gavin M.K., Forrester W.C., Garriga G. The role of C. elegans Ena/VASP homolog UNC-34 in neuronal polarity and motility. Dev. Biol. 2010, 344:94-106.
12. Fujisawa K., Wrana J.L., Culotti J.G. The slit receptor EVA-1 coactivates a SAX-3/Robo mediated guidance signal in C. elegans. Science 2007, 317:1934-1938.
13. Gardner R.G., Nelson Z.W., Gottschling D.E. Degradation-mediated protein quality control in the nucleus. Cell 2005, 120:803-815.
14. Gelsthorpe M.E., Baumann N., Millard E., Gale S.E., Langmade S.J., Schaffer J.E., Ory D.S. Niemann-Pick type C1 I1061T mutant encodes a functional protein that is selected for endoplasmic reticulum-associated degradation due to protein misfolding. J.Biol. Chem. 2008, 283:8229-8236.
15. Georgiou M., Tear G. Commissureless is required both in commissural neurones and midline cells for axon guidance across the midline. Development 2002, 129:2947-2956.
16. Gidalevitz T., Prahlad V., Morimoto R.I. The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb. Perspect. Biol. 2011, 3:a009704.
17. Gurskaya N.G., Verkhusha V.V., Shcheglov A.S., Staroverov D.B., Chepurnykh T.V., Fradkov A.F., Lukyanov S., Lukyanov K.A. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 2006, 24:461-465.
18. Hao J.C., Yu T.W., Fujisawa K., Culotti J.G., Gengyo-Ando K., Mitani S., Moulder G., Barstead R., Tessier-Lavigne M., Bargmann C.I. C.elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron 2001, 32:25-38.
19. Heck J.W., Cheung S.K., Hampton R.Y. Cytoplasmic protein quality control degradation mediated by parallel actions of the E3 ubiquitin ligases Ubr1 and San1. Proc. Natl. Acad. Sci. USA 2010, 107:1106-1111.
20. Hua Z., Vierstra R.D. The cullin-RING ubiquitin-protein ligases. Annu. Rev. Plant Biol. 2011, 62:299-334.
21. Irobi J., Van Impe K., Seeman P., Jordanova A., Dierick I., Verpoorten N., Michalik A., De Vriendt E., Jacobs A., Van Gerwen V., et al. Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy. Nat. Genet. 2004, 36:597-601.
22. Jarosz D.F., Taipale M., Lindquist S. Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu. Rev. Genet. 2010, 44:189-216.
23. Jen J.C., Chan W.M., Bosley T.M., Wan J., Carr J.R., Rüb U., Shattuck D., Salamon G., Kudo L.C., Ou J., et al. Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science 2004, 304:1509-1513.
24. Keleman K., Rajagopalan S., Cleppien D., Teis D., Paiha K., Huber L.A., Technau G.M., Dickson B.J. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 2002, 110:415-427.
25. Kjaer S., Ibáñez C.F. Intrinsic susceptibility to misfolding of a hot-spot for Hirschsprung disease mutations in the ectodomain of RET. Hum. Mol. Genet. 2003, 12:2133-2144.
26. Lee D.Y., Brown E.J. Ubiquilins in the crosstalk among proteolytic pathways. Biol. Chem. 2012, 393:441-447.
27. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
28. Lim J., Hao T., Shaw C., Patel A.J., Szabó G., Rual J.F., Fisk C.J., Li N., Smolyar A., Hill D.E., et al. A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell 2006, 125:801-814.
29. Lukacs G.L., Verkman A.S. CFTR: folding, misfolding and correcting the δF508 conformational defect. Trends Mol. Med. 2012, 18:81-91.
30. Mahrour N., Redwine W.B., Florens L., Swanson S.K., Martin-Brown S., Bradford W.D., Staehling-Hampton K., Washburn M.P., Conaway R.C., Conaway J.W. Characterization of Cullin-box sequences that direct recruitment of Cul2-Rbx1 and Cul5-Rbx2 modules to Elongin BC-based ubiquitin ligases. J.Biol. Chem. 2008, 283:8005-8013.
31. Makarova K.S., Aravind L., Koonin E.V. SWIM, a novel Zn-chelating domain present in bacteria, archaea and eukaryotes. Trends Biochem. Sci. 2002, 27:384-386.
32. Morlot C., Thielens N.M., Ravelli R.B., Hemrika W., Romijn R.A., Gros P., Cusack S., McCarthy A.A. Structural insights into the Slit-Robo complex. Proc. Natl. Acad. Sci. USA 2007, 104:14923-14928.
33. Najarro E.H., Wong L., Zhen M., Carpio E.P., Goncharov A., Garriga G., Lundquist E.A., Jin Y., Ackley B.D. Caenorhabditis elegans flamingo cadherin fmi-1 regulates GABAergic neuronal development. J.Neurosci. 2012, 32:4196-4211.
34. Pedersen C.B., Bross P., Winter V.S., Corydon T.J., Bolund L., Bartlett K., Vockley J., Gregersen N. Misfolding, degradation, and aggregation of variant proteins. The molecular pathogenesis of short chain acyl-CoA dehydrogenase (SCAD) deficiency. J.Biol. Chem. 2003, 278:47449-47458.
35. Rosenbaum J.C., Fredrickson E.K., Oeser M.L., Garrett-Engele C.M., Locke M.N., Richardson L.A., Nelson Z.W., Hetrick E.D., Milac T.I., Gottschling D.E., Gardner R.G. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol. Cell 2011, 41:93-106.
36. Roth J., Zuber C., Park S., Jang I., Lee Y., Kysela K.G., Le Fourn V., Santimaria R., Guhl B., Cho J.W. Protein N-glycosylation, protein folding, and protein quality control. Mol. Cells 2010, 30:497-506.
37. Schubert U., Antón L.C., Gibbs J., Norbury C.C., Yewdell J.W., Bennink J.R. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000, 404:770-774.
38. Sharma H.S., Hoopes P.J. Hyperthermia induced pathophysiology of the central nervous system. Int. J. Hyperthermia 2003, 19:325-354.
39. Singh N., Zanusso G., Chen S.G., Fujioka H., Richardson S., Gambetti P., Petersen R.B. Prion protein aggregation reverted by low temperature in transfected cells carrying a prion protein gene mutation. J.Biol. Chem. 1997, 272:28461-28470.
40. Skovronsky D.M., Lee V.M., Trojanowski J.Q. Neurodegenerative diseases: new concepts of pathogenesis and their therapeutic implications. Annu. Rev. Pathol. 2006, 1:151-170.
41. Tabas I., Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 2011, 13:184-190.
42. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
43. Taipale M., Krykbaeva I., Koeva M., Kayatekin C., Westover K.D., Karras G.I., Lindquist S. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 2012, 150:987-1001.
44. Tyedmers J., Mogk A., Bukau B. Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 2010, 11:777-788.
45. Vollrath D., Liu Y. Temperature sensitive secretion of mutant myocilins. Exp. Eye Res. 2006, 82:1030-1036.
46. Voss A.K., Thomas T., Gruss P. Mice lacking HSP90β fail to develop a placental labyrinth. Development 2000, 127:1-11.
47. Yan S., Sun X., Xiang B., Cang H., Kang X., Chen Y., Li H., Shi G., Yeh E.T., Wang B., et al. Redox regulation of the stability of the SUMO protease SENP3 via interactions with CHIP and Hsp90. EMBO J. 2010, 29:3773-3786.
48. Yochem J., Gu T., Han M. A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis. Genetics 1998, 149:1323-1334.
49. Yuasa-Kawada J., Kinoshita-Kawada M., Wu G., Rao Y., Wu J.Y. Midline crossing and Slit responsiveness of commissural axons require USP33. Nat. Neurosci. 2009, 12:1087-1089.
50. Zallen J.A., Yi B.A., Bargmann C.I. The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C.elegans. Cell 1998, 92:217-227.